Faculty of Biological Sciences, University of Leeds

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Primate Behaviour

Dr. Bill Sellers

Up till know I've talked mostly about physical
features: how they apply to extant primates; how we use them for
classification; how they apply to the fossil record. But human evolution
isn't simply about how we have changed physically over the last 70
million years, but also about how our behaviour has changed.

If I
asked you to define what is meant by the term "human", you could
probably (hopefully) give me a list of shared, derived characters that
anatomically define us. But at a philosophical level, I would hope that
what you'd be really proud of is not that we normally walk bipedally,
but that we can reason and imagine. Old Descartes put it succinctly: "I
think, therefore I am" (but not quite in this context).

This
lecture isn't about human behaviour per se, but about primate
behaviour in general (and animal behaviour too), since just as we can
use the morphology of living primates to give us clues and insights into
the morphology of human ancestors, so we hope that the behaviours of
non-human primates (NHPs) will be similarly enlightening for the
behaviour of our ancestors.

As I said, the study of primate behaviour is essential for
giving us clues to the possible behaviours of our ancestors. However, it
is an important study in its own right. It has now become our
responsibility to manage much of the life on this planet, and in order
to preserve what we currently have, we need to understand what the
animals require in terms of space, diet, group organisation etc. to make
sure that we leave sufficient wild habitats, or, if absolutely
necessary, recreate suitable habitats in captivity.

The most rewarding studies for conservation purposes are
studies of the animals in their natural habitat. Studying an animal in
relation to its environment in this way is called behavioural ecology.
Obviously, defining an environment is a complex thing to do, including
both biotic and abiotic factors.

Factors that might
need to be taken into account include:

1. Quantity and quality of
different kinds of food

2. Distribution of food resources

3. Distribution
of water

4. Distribution and types of predators

5. Distribution
of sleeping sites

6. Activity patterns (nocturnal/diurnal)

7. Relationship
with other (non-predator) species

8. Impacts of human activity

These (and other) variables form a complex and dynamic web of
interactions and it is the job of the behavioural ecologist to try and
make some sense of them all.

For example, one variable that can
be measures is average group size. It is often assumed that large groups
can form in response to predator pressure (for example baboons living on
the African savannah), where having more members in the group increases
the likelihood of predator detection, and the animals may be able to
gang together to drive off some of the predators.

However, there
may be other strategies that can be pursued. The slender loris, for
example, is largely solitary and nocturnal, and avoids predators by
hiding, rather than attempting to run away.

Socio-biology is to
some extent an attempt to quantify behavioural ecology. Behavioural
ecology attempts to identify a set of variables that have a qualitative
effect on a behaviour: "an increase in predation pressure leads to an
increase in group size." Socio-biology is an approach that says: "with a
predator density of 2 lions per square kilometre, I predict that the
group size will be 15 individuals." Obviously, this is a testable
prediction and if the results are found to agree, it makes the cause and
effect argument much harder to refute.

How does it work?
Socio-biologist postulate that behaviour is an inherited trait, that is
under the influence of natural selection much like any other trait
(trait = phenotype). However, for it to be inherited, it must be
influenced by genetics, and if this is the case, then its evolutionary
impact can be directly measured by its impact on reproductive success.

Individuals whose genotype lead to higher reproductive success are
fitter (by definition), and will pass these genes on at a faster rate,
so these genes will spread (become fixed) in a population.

This
is fine for animals where particular behaviours can be linked to genes
(this has been done in fruit flies and some marine snails), but is open
to question in a situation (as in primates) where much observed
behaviour is a result of the environment (learning) rather than being
innate (genetic), though even for learned behaviours, an animal is very
likely to imitate its parents as opposed to other animals, so in this
respect, behaviour is still inherited. And the behaviour itself, if
widely copied, will spread through the population.

For the
numerical predictions to work, the behaviour must be very largely
inherited. It tends to work well with things where the animal is seen to
have rather limited "conscious" control, such as clutch size in birds,
interbirth interval in primates or sex of offspring. Behaviours are
known to affect these things, but they seem to operate at a "low"
cognitive level. They don't require thought.

However, the
socio-ecological paradigm is very useful. It enables us to look at
behaviours as a set of strategies in a game, with maximising individual
reproductive success as the goal. We can then use game theory
predictions in an attempt to explain the options available and their
individual costs and benefits.

For example, look at the case of
infanticide which is seen in a great many mammals, including primates.
Hanuman langurs (India) live in social groups consisting of a single
male and several females. Periodically, the resident male in these
groups is challenged by an outsider, and if the outsider is successful
in beating the resident, he takes over, and generally kills all the
infants currently in the group.

Why? This seems to be bad for the
species... But under the socio-biological tenet, we see that being good
for the species (so called "group selection") is not important. To
understand this behaviour, we must consider the male attempting to
maximise his reproductive success. By killing the infants, he stops the
mothers from continuing to lactate, and that way they become sexually
receptive again quicker. He will then start to father his own infants
sooner, and will therefore produce more offspring before he is in turn
ousted from his position as the resident male in the group.

And that neatly brings us onto the question of reproductive
strategies. In animals, the ultimate goal is to maximise reproductive
success. In primates, this is generally achieved in females by having
few young, and investing a great deal of time and effort into rearing
them (lactating etc.). This large investment in a few offspring is often
described as K-selected. Male primates, in general, take very little
interest in helping to rear offspring. Their approach to maximising
their reproductive success is to father as many offspring as possible
and not to invest much in individual ones. This is often described as
r-selection (the letters K and r are from a famous population dynamics
equation that everyone forgets about).

There is certainly evidence
that K-selection has increased in human evolution characterised by fewer
offspring and prolonged periods of infancy. It is possible that the
investment by males has also increased (but then again...).

There
is an interesting strategy that has been reported on mangabeys. There
appear to be 2 sorts of males: one very large and aggressive; the other
smaller and more similar in size to a female or a juvenile. The large
males are seen to mate very openly, whereas the smaller ones are seen to
mate surreptitiously. It remains to be seen which strategy is the most
successful in the long run since it's only with the advent of DNA
fingerprinting that we can be certain about paternity.

There are
some caveats with socio-biology. It relies very heavily on the
assumption that animals are indeed well adapted to their environments,
and whist this is probably often the case, it isn't necessarily so.
However, if we are forced to conclude that an animal isn't well adapted
then there doesn't seen any way forward, so we have to start assuming
that is, and only conclude that an animal is the way it is because of
history, and taxonomic inertia (slow change rates) as a last resort.

Primates, as (mostly) group
living animals tend to form what are known as "dominance hierarchies".
Animals higher in the hierarchy tend to displace lower ranked
individuals from resources (mates, space, food). They tend to have
higher reproductive success (either by mating more often, or by having
more resources to invest in their offspring). The hierarchy is not fixed
and depends on a number of changing factors (age, sex, aggression,
intelligence perhaps), and may also depend on the support of others.

The
rank is learned through play, agonistic interactions and affiliative
interactions (and rather tautological, that's exactly how it's measured
too). This maintenance of social position, and social knowledge of ones
rank is one of the postulated theories for why humans have been forced
to evolve large brains.

This is a common primate
activity. Allogrooming (others) is an important affiliative mechanism.
It can be used to strengthen links: subordinate animals tend to groom
more dominate ones; males groom females for sexual access. Or for more
practical purposes: mothers grooming infants to keep their fur clean? It
is certainly the cement that keeps the primate social structure
together.

This includes scents;
body postures; gestures; vocalisations. Some of these appear to be
autonomic responses indicating emotional states: fear, excitement,
confidence, anger. Others seem to have a more specific purpose: loud
ranging calls in Indri, howler monkeys and gibbons; quiet contact calls
in lemurs to keep the group together; fear calls in lost infants, or on
spotting predators. From our human perspective, we often find it easier
to associate sounds with specific meaning, but among NHPs, gestures and
actions are often used. Presentation and mounting behaviour is often
used to diffuse potentially aggressive situations. Yawns exposing teeth
are often threats, as is direct eye contact. Apparently this can cause
problems when looking at baboons with binoculars: the front lenses look
like bigger than normal eyes and this is seen as the observer being very
aggressive.

Facial expression is important too. It's very obvious in
chimps: their expression often appear all to human-like; but other
primates also use stereotyped eyelid flashes or lip slaps.

In
addition, there has recently been a great deal of success teaching
chimps human language. This was initially American sign language, but
has now been extended through the use of modified computer keyboards to
really very high levels of sophistication (especially Kanzi, a pygmy
chimp).

In all primates,
except for humans (and perhaps chimps), the females are seasonally, or
cyclically receptive. This is usually associated with visual changes
such as perianal swelling, so that is clear when the females are in
heat. Pair bonding of any sort is rare among primates, though gibbons
seem to be lifelong monogamists, and some new world monkey groups, such
as marmosets, have only one reproductively active pair in any group.
Chimps, especially pygmy chimps, have been seen to have consortships of
several weeks where copulation is frequent, but there is still no good
evidence for paternal care of the infants.

This is the basic social group for many primates. It has been
observed that this mother infant bonding is needed to allow the infant
to be able to interact properly as an adult, and, if female, to be able
to cope with offspring. This is one of the big problems with zoo animals
where an individual has been hand reared by keepers. In some primates,
this mother infant closeness continues after infancy. The females
remaining in the group as a "matriline" and the males dispersing to
other groups. The combined power of one of these female bonded
matrilines is enough for the group of females to be more dominant than
the alpha male, even though he is much bigger than an individual member.

As mentioned before, many behaviours exist to keep the group
structure running smoothly for the members of the group. There are
occasions though when these behaviours (especially aggression) are
directed outside the group. Baboons gang up to repel attacks by hyenas,
and chimps have been known to systematically gang up on and destroy
neighbouring groups of chimps.

One interesting argument here, is that
the development of bipedalism has been seen by some to be driven by a
root as an aggressive, dominance display behaviour. This is the gorilla
standing bipedally and banging his chest, or a male chimp bipedally
charging a subordinate. Most people would probably consider this to be
an effect of a bipedal ability, rather than the cause.

This is learned behaviour that is passed from generation to
generation. You will hear a lot about this in humans, but it has been
observed in primates too. One prime example is a group of Japanese
macaques, where one individual accidentally learned that the sweet
potatoes that they were being fed tasted better if the sand was washed
off (this is not a normal food for these animals). This behaviour has
now spread through the whole group, and is being passed on to infants.
It is now part of their culture. Tool use abilities are often thought to
be acquired and passed on in this way too - for example, termite fishing
in chimps.

I've mentioned a lot about behaviours without mentioning much
about cognition. This is the amount of thought that went into a
behaviour. There is a world of difference between an animal hitting a
nut with a rock and cracking it by accident, and an animal thinking to
itself: "I can't bite into this nut. I know, I need something to use as
a hammer to crack it." However, it can be very difficult coming up with
experiments to differentiate these two.

We can easily test mental
skills such as recall and discrimination: e.g.. Wisconsin general test
apparatus and various training experiments. But it's much harder to work
out the degree of thought required. This is still a big problem in
evaluating the status of great apes. Just how nearly "sentient" are
they?

Another feature that has come to light recently is
"Machievellian Intelligence". Work especially with baboons seems to
indicate that there is a lot of deliberate social deception going on:
sneaky mating; passing the blame onto others; using infants for defence.
This seems very complicated behaviourally, but again, it can (just
about) be explained in a fairly minimally cognitive way.

Altruism
of various sorts is also found in certain primates. The animals team up
to gain various goals, whether it's hunting in chimps, or mate access in
baboons. This would also seem to require a degree of cognition.

The
signing chimp, Washoe, and the computer aided communication of Kanzi
also indicate a high level of intelligence. An interesting fact is that
these language trained chimps do much better in the standardised
intelligence tests too, indicating that we probably underestimate
primate intelligence (primates are not all that interested in the colour
of pencils, they want to know which of their friends are sleeping with
each other - sound familiar?)

This is a thorny problem, with deep
moral and political ramifications.

This lecture has
concentrated on social behaviour, because, to some extent, it's what's
most interesting and also what makes NHPs so like us. However, behaviour
also include locomotion (running, jumping, walking and climbing) and
specifics of foraging behaviour. Socio-biological principles give us the
tools to objectively investigate these things, but we shouldn't be
blinded by the perfection of the method. In the end, most behavioural
studies just give clues to the big picture, and the picture itself needs
to be pieced together like a jigsaw. And like most of these things, it
is open to interpretation too.